Species assembly in model ecosystems, I: Analysis of the population model and the invasion dynamics

Recently we have introduced a simplified model of ecosystem assembly (Capitán et al., 2009) for which we are able to map out all assembly pathways generated by external invasions in an exact manner. In this paper we provide a deeper analysis of the model, obtaining analytical results and introducing some approximations which allow us to reconstruct the results of our previous work. In particular, we show that the population dynamics equations of a very general class of trophic-level structured food-web have an unique interior equilibrium point which is globally stable. We show analytically that communities found as end states of the assembly process are pyramidal and we find that the equilibrium abundance of any species at any trophic level is approximately inversely proportional to the number of species in that level. We also find that the per capita growth rate of a top predator invading a resident community is key to understand the appearance of complex end states reported in our previous work. The sign of these rates allows us to separate regions in the space of parameters where the end state is either a single community or a complex set containing more than one community. We have also built up analytical approximations to the time evolution of species abundances that allow us to determine, with high accuracy, the sequence of extinctions that an invasion may cause. Finally we apply this analysis to obtain the communities in the end states. To test the accuracy of the transition probability matrix generated by this analytical procedure for the end states, we have compared averages over those sets with those obtained from the graph derived by numerical integration of the Lotka-Volterra equations. The agreement is excellent.     

Testing whether productivity mediates the occurrence of alternate stable states and assembly cycles in a model microcosm system

When do initial conditions, which reflect the assembly history of a community, affect the final community state? Comparative field studies and recent theory suggest that initial conditions matter at high productivity, because uninvasible alternate stable states and assembly cycles are more likely at high productivity. However, this prediction and the mechanisms behind it have not been tested experimentally. An alternative hypothesis is that initial conditions are relatively unimportant, and that communities generally are comprised of species with appropriate traits, which might vary with productivity. I assembled communities of protists and rotifers in laboratory microcosms from a species‐rich, trophically‐diverse species pool using all possible combinations of two initial conditions and four productivity levels. After communities approached their final states, invasions by the species that initially failed to persist tested the invasibility of those final states and tested for assembly cycles. I also examined how local (within‐microcosm) diversity and regional diversity (total species richness of all microcosms of a given productivity level) varied with productivity. Comparative field work has used such scale‐dependent diversity–productivity relationships as evidence for effects of assembly history. Productivity had a modest effect on final pre‐invasion species composition, while initial conditions had a very weak effect. Most invasions failed, and the frequency of successful invasions and of post‐invasion extinctions did not vary with productivity. Instead, species that were present most frequently pre‐invasion were also the most successful invaders, and the least‐likely species to go extinct post‐invasion. Local and regional richness did not vary substantially with productivity. Overall, the results suggest that final communities are predictably comprised of species with appropriate traits, and are not an unpredictable outcome of initial conditions.     

From simple rules to cycling in community assembly

Simulation studies of community assembly have frequently observed two related phenomena: (1) the humpty dumpty effect in which communities can not be reconstructed by "sequential" invasions (i.e. single species invasions separated by long intervals of time) and (2) cycling between sub-communities. To better understand the mechanisms underlying these phenomena, we analyze a system consisting of two predators and two prey competing for a shared resource. We show how simple dominance rules (i.e. R^* and P^* rules) lead to cycling between sub-communities consisting of predator–prey pairs; predator and prey invasions alternatively lead to prey displacement via apparent competition and predator displacement via exploitative competition. We also show that these cycles are often dynamically unstable in the population phase space. More specifically, while for too slow invasion rates (i.e. "sequential" invasions) the system cycles indefinitely, faster invasion rates lead to coexistence of all species. In the later case, the assembly dynamics exhibit transient cycling between predator-prey subcommunities and the length of these transients decreases with the invasion rate and increases with habitat productivity.     

Past states of continuous-time Markov models for ecological communities

Discrete-time Markov chains are often used to model communities of sessile organisms. The community is described by a set of discrete states, which may represent species or groups of species. Transitions between states are modelled using a stochastic matrix. A recent study showed how the time-reversal of such a Markov chain can be used to estimate the distribution of time since the last occurrence of some state of interest (such as empty space) at a point, given the current state of the point. However, if the underlying process operates in continuous time but is observed at regular intervals, this distribution describes the time since the last possible observation of the state of interest, rather than the time since its last occurrence. We show how to obtain the distribution of time since the last occurrence of a state of interest for a continuous-time homogeneous Markov chain. The expected time since the last occurrence of an initial state can be interpreted as a measure of the successional rank of a state. We show how to distinguish between different ways in which a state can have high successional rank. We apply our results to a marine subtidal community.     

Community assembly along a species pool gradient: implications for multiple-scale patterns of species diversity

Various ecological processes influence patterns of species diversity at multiple spatial scales. One process that is potentially important but rarely considered is community assembly. I assembled model communities using species pools of differing size to examine how the history of community assembly may affect multi-scale diversity patterns. The model contained three scales at which diversity could be measured: local community, metacommunity, and species pool. Local species saturation occurred, as expected from the competition and predation built in the model. However, local communities did not become resistant to invasions except when the species pool was very small. Depending on dispersal rate and trophic level, the larger the species pool, the harder it was to predict which species invades which local community at a given time. Consequently, local-community dissimilarity maintained by assembly history increased linearly with pool size, even though local diversity was decoupled from pool size. These results have two implications for multi-scale diversity patterns. First, assembly history may provide an explanation for scale-dependent relationships between local and regional diversity: assembly causes the relationship to be curvilinear at one scale (local community), while linear at another (metacommunity). Second, assembly history influences how -diversity is partitioned into - and -diversity: assembly causes the relative contribution of to increase with pool size. Overall, this study suggests that community assembly history interacts with species pool size to regulate multi-scale patterns of species diversity.     

Non-native earthworms alter the assembly of a meadow plant community

Non-native earthworms can alter ecosystems by modifying soil structure, depredating seeds and seedlings, and consuming soil organic matter, yet the initial responses of plant communities to earthworm invasions remain poorly understood. We assessed the effect of non-native earthworms on seedling survival during germination and after establishment using six native and six non-native plant species grown from seed in single- and multi-species experimental mesocosms. We examined the extent to which earthworms (1) influenced seedling survival, (2) selectively depredated native versus non-native plants, (3) impacted establishment based on seed size and/or root morphology, and (4) shaped community assembly. The effect of earthworms on seedling survival varied temporally and among species but inconsistently with respect to species origin. Differences in seed/seedling survival translated to changes in community assembly. Earthworms tended to reduce species abundance, richness, evenness, and diversity in multi-species mesocosms and led to the divergence of communities by treatment. In general, species with large seeds and fibrous roots dominated communities with earthworms present, whereas species with small seeds and taproots only persisted in multi-species mesocosms without earthworms. Our findings suggest that earthworms act as ecological filters in the early stages of invasion to shape community composition based on plant morphological traits.

     

Is the assembly of ant communities mediated by parasitoids?

Studies of species interactions in ant communities have been a major source of evidence for the importance of interspecific competition in natural communities. One consequence of the overwhelming evidence for competition in ant communities is that the role of such "top-down" processes as predation and parasitism has been ignored. Recent evidence, however, suggests that the composition and dynamics of ant communities are influenced by highly specialized parasitoids that mediate the outcome of competition among ant species. Here I review this evidence and develop a general framework for integrating the roles of competition and parasitism in the assembly of ant communities. I then use invasions by the red imported fire ant ( Solenopsis wagneri ) and the Argentine ant ( Linepithema humile ) to show how this new framework can be used to develop testable hypotheses regarding the ecological success (or failure) of invasive ant species.     

Graphs, random sums, and sojourn time distributions, with application to ion-channel modeling.

This paper considers the distribution of a sojourn time in a class of states of a stochastic process having finite discrete state space where sojourn times in any individual state are independent and identically distributed, and transitions between states follow a Markov chain. The state space and possible transitions of the process are represented by a graph. Class sojourn time distributions are derived by modifying this graph using 'composition' of states, defining a new Markov chain on the modified graph, and expressing the sojourn time in a composition state as a random sum. Appropriate compositions are chosen according to the possible "cores" of sojourns in the particular class, where a core describes the structure of a sojourn in terms of a single state or a chain in the original graph. Graph methods provide an algorithmic basis for the derivation, which can be simplified by using symmetry results. Models of ion-channel kinetics are used throughout for illustration; class sojourn time distributions are important in such models because individual states are often indistinguishable experimentally. Markov processes are the special case where sojourn times in individual states are exponentially distributed. In this case kinetic parameter estimation based on the observed class sojourn time distribution is briefly discussed; explicit estimating equations applicable to sequential models of nicotinic receptor kinetics are given.     

Community disassembly under global change: Evidence in favor of the stress‐dominance hypothesis

Ecological theory suggests that communities are not random combinations of species but rather the results of community assembly processes filtering and sorting species that are able to coexist together. To date, such processes (i.e., assembly rules) have been inferred from observed spatial patterns of biodiversity combined with null model approaches, but relatively few attempts have been made to assess how these processes may be changing through time. Specifically, in the context of the ongoing biodiversity crisis and global change, understanding how processes shaping communities may be changing and identifying the potential drivers underlying these changes become increasingly critical. Here, we used time series of 460 French freshwater fish communities and assessed both functional and phylogenetic diversity patterns to determine the relative importance of two key assembly rules (i.e., habitat filtering and limiting similarity) in shaping these communities over the last two decades. We aimed to (a) describe the temporal changes in both functional and phylogenetic diversity patterns, (b) determine to what extent temporal changes in processes inferred through the use of standardized diversity indices were congruent, and (c) test the relationships between the dynamics of assembly rules and both climatic and biotic drivers. Our results revealed that habitat filtering, although already largely predominant over limiting similarity, became more widespread over time. We also highlighted that phylogenetic and trait‐based approaches offered complementary information about temporal changes in assembly rules. Finally, we found that increased environmental harshness over the study period (especially higher seasonality of temperature) led to an increase in habitat filtering and that biological invasions increased functional redundancy within communities. Overall, these findings underlie the need to develop temporal perspectives in community assembly studies, as understanding ongoing temporal changes could provide a better vision about the way communities could respond to future global changes.     

Linking community assembly and structure across scales in a wild mouse parasite community

Understanding what processes drive community structure is fundamental to ecology. Many wild animals are simultaneously infected by multiple parasite species, so host–parasite communities can be valuable tools for investigating connections between community structures at multiple scales, as each host can be considered a replicate parasite community. Like free‐living communities, within‐host–parasite communities are hierarchical; ecological interactions between hosts and parasites can occur at multiple scales (e.g., host community, host population, parasite community within the host), therefore, both extrinsic and intrinsic processes can determine parasite community structure. We combine analyses of community structure and assembly at both the host population and individual scales using extensive datasets on wild wood mice (Apodemus sylvaticus) and their parasite community. An analysis of parasite community nestedness at the host population scale provided predictions about the order of infection at the individual scale, which were then tested using parasite community assembly data from individual hosts from the same populations. Nestedness analyses revealed parasite communities were significantly more structured than random. However, observed nestedness did not differ from null models in which parasite species abundance was kept constant. We did not find consistency between observed community structure at the host population scale and within‐host order of infection. Multi‐state Markov models of parasite community assembly showed that a host's likelihood of infection with one parasite did not consistently follow previous infection by a different parasite species, suggesting there is not a deterministic order of infection among the species we investigated in wild wood mice. Our results demonstrate that patterns at one scale (i.e., host population) do not reliably predict processes at another scale (i.e., individual host), and that neutral or stochastic processes may be driving the patterns of nestedness observed in these communities. We suggest that experimental approaches that manipulate parasite communities are needed to better link processes at multiple ecological scales.     

Symmetric assembly and disassembly processes in an ecological network

The processes whereby ecological networks emerge, persist and decay throughout ecosystem development are largely unknown. Here we study networks of plant and arbuscular mycorrhizal fungal (AMF) communities along a 120 000 year soil chronosequence, as they undergo assembly (progression) and then disassembly (retrogression). We found that network assembly and disassembly were symmetrical, self‐reinforcing processes that together were capable of generating key attributes of network architecture. Plant and AMF species that had short indirect paths to others in the community (i.e. high centrality), rather than many direct interaction partners (i.e. high degree), were best able to attract new interaction partners and, in the case of AMF species, also to retain existing interactions with plants during retrogression. We then show using simulations that these non‐random patterns of attachment and detachment promote nestedness of the network. These results have implications for predicting extinction sequences, identifying focal points for invasions and suggesting trajectories for restoration.     

Multi-objective optimization of an ecological assembly model

The aim of the present work is to use multi-objective evolutionary algorithms (MOEA) to parameterise an ecological assembly model based on Lotka–Volterra dynamics. In community assembly models, species are introduced from a pool of species according to a sequence of invasion. By manipulating the assembly sequences, we look at the structure of the final communities obtained by a multi-objective process where the goal is to optimize the productivity of the final communities. The MOEA must also meet the constraint that the communities constructed in this fashion have a specified connectance. The Non-dominated Sorting Algorithm (NSGA-II) and the Strength Pareto Evolutionary Algorithm (SPEA2) were employed to optimize sequences according to the multi-objective optimization problem. The results show that the assembly process using optimized sequences generated different community structure than those generated via random sequences. First, the assembled communities are much more productive than those obtained from random sequences. We show that this increase of productivity is due to the degree distribution of the community food web, which was reshaped by the optimization process. In addition, using identical regional species pools the MOEAs were able to generate communities of different expected connectances. These results demonstrate the effectiveness of NSGA-II and SPEA2 for optimizing parameters in ecological models.     

Marine biogeography and ecology: invasions and introductions

Although biogeography and ecology had previously been considered distinct disciplines, this outlook began to change in the early 1990s. Several people expressed interest in creating a link that would help ecologists become more aware of external influences on communities and help biogeographers realize that distribution patterns had their genesis at the community level. They proposed an interdisciplinary approach called macroecology. This concept has been aided by the advent of phylogeography, for a better knowledge of genetic relationships has had great interdisciplinary value. Two areas of research that should obviously benefit from a macroecological approach are: (1) the question of local vs. regional diversity and (2) the question of whether invader species pose a threat to biodiversity. The two questions are related, because both deal with the vulnerability of ecosystems to penetration by invading species. Biogeographers, who have studied the broad oceanic patterns of dispersal and colonization, tend to regard isolated communities as being open to invasion from areas with greater biodiversity. It became evident that many wide‐ranging species were produced in centres of origin, and that the location of communities with respect to such centres had a direct effect on the level of species diversity. Ecologists, in earlier years, thought that a community could become saturated with species and would thereafter be self‐sustaining. But recent research has shown that saturation is probably never achieved and that the assembly of communities and their maintenance is more or less dependent on the invasion of species from elsewhere. The study of invasions that take place in coastal areas, usually the result of ship traffic and/or aquaculture imports, has special importance due to numerous opinions expressed by scientists and policy‐makers that such invasions are a major threat to biodiversity. However, none of the studies so far conducted has identified the extinction of a single, native marine species due to the influence of an exotic invader. Furthermore, fossil evidence of historical invasions does not indicate that invasive species have caused native extinctions or reductions in biodiversity.     

Functional trait assembly through ecological and evolutionary time

A classic community assembly hypothesis is that all guilds must be represented before additional species from any given guild enter the community. We conceptually extend this hypothesis to continuous functional traits, refine the hypothesis with an eco-evolutionary model of interaction network community assembly, and compare the resultant continuous trait assembly rule to empirical data. Our extension of the “guild assembly rule” to continuous functional traits was rejected, in part, because the eco-evolutionary model predicted trait assembly to be characterized by the expansion of trait space and trait/species sorting within trait space. Hence, the guild rule may not be broadly applicable. A “revised” assembly rule did, however, emerge from the eco-evolutionary model: as communities assemble, the range in trait values will increase to a maximum and then remain relatively constant irrespective of further changes in species richness. This rule makes the corollary prediction that the trait range will, on average, be a saturating function of species richness. To determine if the assembly rule is at work in natural communities, we compared this corollary prediction to empirical data. Consistent with our assembly rule, trait “space” (broadly defined) commonly saturates with species richness. Our assembly rule may thus represent a general constraint placed on community assembly. In addition, taxonomic scale similarly influences the predicted and empirically observed relationship between trait “space” and richness. Empirical support for the model’s predictions suggests that studying continuous functional traits in the context of eco-evolutionary models is a powerful approach for elucidating general processes of community assembly.     

Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution

Ecological fitting is the process whereby organisms colonize and persist in novel environments, use novel resources or form novel associations with other species as a result of the suites of traits that they carry at the time they encounter the novel condition. This paper has four major aims. First, we review the original concept of ecological fitting and relate it to the concept of exaptation and current ideas on the positive role of phenotypic plasticity in evolution. Second, we propose phenotypic plasticity, correlated trait evolution and phylogenetic conservatism as specific mechanisms behind ecological fitting. Third, we attempt to operationalize the concept of ecological fitting by providing explicit definitions for terms. From these definitions, we propose a simple conceptual model of ecological fitting. Using this model, we demonstrate the differences and similarities between ecological fitting and ecological resource tracking and illustrate the process in the context of species colonizing new areas and forming novel associations with other species. Finally, we discuss how ecological fitting can be both a precursor to evolutionary diversity or maintainer of evolutionary stasis, depending on conditions. We conclude that ecological fitting is an important concept for understanding topics ranging from the assembly of ecological communities and species associations, to biological invasions, to the evolution of biodiversity.     

Dispersal among local communities does not reduce historical contingencies during metacommunity assembly

Ample evidence suggests that ecological communities can exhibit historical contingencies. However, few studies have explored whether differences in assembly history can generate alternative local community states in metacommunities in which local communities are linked by dispersal. In a protist microcosm experiment, we examined the influence of species colonization history on metacommunity assembly under homogeneous environmental conditions, by manipulating both the sequence of species colonization into local communities and the rate of dispersal among local communities. Whereas the role of dispersal in structuring local communities decreased over time and became non‐significant towards the end of the experiment, species colonization history significantly influenced local communities throughout the experiment. Local communities, regardless of the rate of dispersal among them, exhibited two alternative states characterized by the dominance of different species. The alternative community states, however, emerged in the absence of priority effects that were often associated with alternative community states found in other assembly studies. Rather, they were driven by variation in species interaction strength among local communities with different assembly histories. These results suggest that dispersal among local communities may not necessarily reduce the role of species colonization history in shaping metacommunity assembly, and that differences in species colonization history need to be explicitly considered as an important factor in causing heterogeneous community states in metacommunities.     

Genetic assembly rules and community phenotypes

We present a conceptual construct for a genetic based community assembly rule where the genetic composition of a host plant, or resource, affects the structure of the dependent community. This is related to a genetic similarity rule that states that host plants with similar genetic compositions are hosts to similar arthropod communities. We present preliminary data from the Populus system to support this concept. We review the recent literature to evaluate the current state of the assembly rule concept and interpret a set of previous studies in the context of a genetic assembly rule. We suggest that by incorporating this concept into community ecology we can begin to bring an evolutionary perspective to this discipline.     

Species co-occurrences and neutral models: reassessing J. M. Diamond's assembly rules

The question whether species co-occurrence patterns are non-random has intrigued ecology for more than two decades. Recently Gotelli and McCabe used meta-analysis to show that natural assemblages indeed tend to have non-random species co-occurrence patterns and that these patterns are in line with the predictions of Diamond's assembly rule model. Here I show that neutral ecological drift models are able to generate patterns in line with Diamond's assembly rules and very similar to the empirical results in Gotelli and McCabe. Ecological drift shifted species co-occurrence patterns (measured by C-scores, checkerboard scores and species combination scores) of model species placed into a grid of the 25 cells (sites; metacommunity sizes 5 to 25 species with 100 individuals each) significantly from an initial random pattern towards a pattern predicted by the assembly rule model of Diamond. These findings imply that instead of asking whether natural communities are structured according to some assembly rules we should ask whether these non-random patterns are generated by species interactions or by stochastic drift processes.     

Community assembly, stability and signatures of dynamical constraints on food web structure

To understand the dynamics of natural species communities, a major challenge is to quantify the relationship between their assembly, stability, and underlying food web structure. To this end, two complementary aspects of food web structure can be related to community stability: sign structure, which refers to the distributions of trophic links irrespective of interaction strengths, and interaction strength structure, which refers to the distributions of interaction strengths with or without consideration of sign structure. In this paper, using data from a set of relatively well documented community food webs, I show that natural communities generally exhibit a sign structure that renders their stability sensitive to interaction strengths. Using a Lotka-Volterra type population dynamical model, I then show that in such communities, individual consumer species with high values of a measure of their total biomass acquisition rate, which I term “weighted generality”, tend to undermine community stability. Thus consumer species’ trophic modules (a species and all its resource links) should be “selected” through repeated immigrations and extinctions during assembly into configurations that increase the probability of stable coexistence within the constraints of the community's trophic sign structure. The presence of such constraints can be detected by the incidence and strength of certain non-random structural characteristics. These structural signatures of dynamical constraints are readily measurable, and can be used to gauge the importance of interaction-driven dynamical constraints on communities during and after assembly in natural communities.     

Community assembly time and the relationship between local and regional species richness

Many previous studies have assumed that a linear relationship between local and regional species richness indicates that communities are limited by regional processes, while a saturating relationship suggests that species interactions restrict local richness. We show theoretically that the relationship between local and regional richness changes in a consistent fashion with assembly time in interacting communities. Communities show saturation in their early assembly stages because only a subset of the regional pool may colonize a locality. At intermediate assembly times, communities will appear unsaturated until significant competitive exclusion occurs. Finally, when communities reach equilibrium, we found saturation as a result of resource competition resulting in the dominance of a limited number of species. We show that habitat size and species fecundity are important in determining the time needed for the community to reach equilibrium and thus affect the relationship between local and regional species richness. Our results suggest the number of coexisting species is a function of local and regional processes whose relative influences might vary over time and that research using the relationship between local and regional species richness to infer mechanisms limiting species richness must have knowledge of the assembly time of the community.